Iron Uptake and Homeostasis in Microorganisms

Preface. Iron is considered to be a minor element employed, in a variety of forms, by nearly all living organisms. In some cases, it is utilised in large quantities, for instance for the formation of magnetosomes within magnetotactic bacteria or during use of iron as a respiratory donor or acceptor by iron oxidising or reducing bacteria. However, in most cases the role of iron is restricted to its use as a cofactor or prosthetic group assisting the biological activity of many different types of protein. The key metabolic processes that are dependent on iron as a cofactor are numerous; they include respiration, light harvesting, nitrogen fixation, the Krebs cycle, redox stress resistance, amino acid synthesis and oxygen transport. Indeed, it is clear that Life in its current form would be impossible in the absence of iron. One of the main reasons for the reliance of Life upon this metal is the ability of iron to exist in multiple redox states, in particular the relatively stable ferrous (Fe2+) and ferric (Fe3+) forms. The availability of these stable oxidation states allows iron to engage in redox reactions over a wide range of midpoint potentials, depending on the coordination environment, making it an extremely adaptable mediator of electron exchange processes. Iron is also one of the most common elements within the Earth’s crust (5% abundance) and thus is considered to have been readily available when Life evolved on our early, anaerobic planet. However, as oxygen accumulated (the ‘Great oxidation event’) within the atmosphere some 2.4 billion years ago, and as the oceans became less acidic, the iron within primordial oceans was converted from its soluble reduced form to its weakly-soluble oxidised ferric form, which precipitated (~1.8 billion years ago) to form the ‘banded iron formations’ (BIFs) observed today in Precambrian sedimentary rocks around the world. These BIFs provide a geological record marking a transition point away from the ancient anaerobic world towards modern aerobic Earth. They also indicate a period over which the bio-availability of iron shifted from abundance to limitation, a condition that extends to the modern day. Thus, it is considered likely that the vast majority of extant organisms face the common problem of securing sufficient iron from their environment – a problem that Life on Earth has had to cope with for some 2 billion years. This struggle for iron is exemplified by the competition for this metal amongst co-habiting microorganisms who resort to stealing (pirating) each others iron supplies! The reliance of micro-organisms upon iron can be disadvantageous to them, and to our innate immune system it represents a chink in the microbial armour, offering an opportunity that can be exploited to ward off pathogenic invaders. In order to infect body tissues and cause disease, pathogens must secure all their iron from the host. To fight such infections, the host specifically withdraws available iron through the action of various iron depleting processes (e.g. the release of lactoferrin and lipocalin-2) – this represents an important strategy in our defence against disease. However, pathogens are frequently able to deploy iron acquisition systems that target host iron sources such as transferrin, lactoferrin and hemoproteins, and thus counteract the iron-withdrawal approaches of the host. Inactivation of such host-targeting iron-uptake systems often attenuates the pathogenicity of the invading microbe, illustrating the importance of ‘the battle for iron’ in the infection process. The role of iron sequestration systems in facilitating microbial infections has been a major driving force in research aimed at unravelling the complexities of microbial iron transport processes. But also, the intricacy of such systems offers a challenge that stimulates the curiosity. One such challenge is to understand how balanced levels of free iron within the cytosol are achieved in a way that avoids toxicity whilst providing sufficient levels for metabolic purposes – this is a requirement that all organisms have to meet. Although the systems involved in achieving this balance can be highly variable amongst different microorganisms, the overall strategy is common. On a coarse level, the homeostatic control of cellular iron is maintained through strict control of the uptake, storage and utilisation of available iron, and is co-ordinated by integrated iron-regulatory networks. However, much yet remains to be discovered concerning the fine details of these different iron regulatory processes. As already indicated, perhaps the most difficult task in maintaining iron homeostasis is simply the procurement of sufficient iron from external sources. The importance of this problem is demonstrated by the plethora of distinct iron transporters often found within a single bacterium, each targeting different forms (complex or redox state) of iron or a different environmental condition. Thus, microbes devote considerable cellular resource to securing iron from their surroundings, reflecting how successful acquisition of iron can be crucial in the competition for survival. The aim of this book is provide the reader with an overview of iron transport processes within a range of microorganisms and to provide an indication of how microbial iron levels are controlled. This aim is promoted through the inclusion of expert reviews on several well studied examples that illustrate the current state of play concerning our comprehension of how iron is translocated into the bacterial (or fungal) cell and how iron homeostasis is controlled within microbes. The first two chapters (1-2) consider the general properties of microbial iron-chelating compounds (known as ‘siderophores’), and the mechanisms used by bacteria to acquire haem and utilise it as an iron source. The following twelve chapters (3-14) focus on specific types of microorganism that are of key interest, covering both an array of pathogens for humans, animals and plants (e.g. species of Bordetella, Shigella, , Erwinia, Vibrio, Aeromonas, Francisella, Campylobacter and Staphylococci, and EHEC) as well as a number of prominent non-pathogens (e.g. the rhizobia, E. coli K-12, Bacteroides spp., cyanobacteria, Bacillus spp. and yeasts). The chapters relay the common themes in microbial iron uptake approaches (e.g. the use of siderophores, TonB-dependent transporters, and ABC transport systems), but also highlight many distinctions (such as use of different types iron regulator and the impact of the presence/absence of a cell wall) in the strategies employed. We hope that those both within and outside the field will find this book useful, stimulating and interesting. We intend that it will provide a source for reference that will assist relevant researchers and provide an entry point for those initiating their studies within this subject. Finally, it is important that we acknowledge and thank wholeheartedly the many contributors who have provided the 14 excellent chapters from which this book is composed. Without their considerable efforts, this book, and the understanding that it relays, would not have been possible. Simon C Andrews and Pierre Cornelis

Increased temperature sensitivity of net DOC production from ombrotrophic peat due to water table draw-down.

The production and release of dissolved organic carbon (DOC) from peat soils is thought to be sensitive to changes in climate, specifically changes in temperature and rainfall. However, little is known about the actual rates of net DOC production in response to temperature and water table draw-down, particularly in comparison to carbon dioxide (CO2) fluxes. To explore these relationships, we carried out a laboratory experiment on intact peat soil cores under controlled temperature and water table conditions to determine the impact and interaction of each of these climatic factors on net DOC production. We found a significant interaction (P < 0.001) between temperature, water table draw-down and net DOC production across the whole soil core (0 to −55 cm depth). This corresponded to an increase in the Q10 (i.e. rise in the rate of net DOC production over a 10 °C range) from 1.84 under high water tables and anaerobic conditions to 3.53 under water table draw-down and aerobic conditions between −10 and − 40 cm depth. However, increases in net DOC production were only seen after water tables recovered to the surface as secondary changes in soil water chemistry driven by sulphur redox reactions decreased DOC solubility, and therefore DOC concentrations, during periods of water table draw-down. Furthermore, net microbial consumption of DOC was also apparent at − 1 cm depth and was an additional cause of declining DOC concentrations during dry periods. Therefore, although increased temperature and decreased rainfall could have a significant effect on net DOC release from peatlands, these climatic effects could be masked by other factors controlling the biological consumption of DOC in addition to soil water chemistry and DOC solubility. These findings highlight both the sensitivity of DOC release from ombrotrophic peat to episodic changes in water table draw-down, and the need to disentangle complex and interacting controls on DOC dynamics to fully understand the impact of environmental change on this system.

Linking carbon and sulphur cycling during simulated drought cycles in peat from six sites across the UK

Water table draw-down is thought to increase peat decomposition and, therefore, DOC release. However, several studies have shown lower DOC concentrations during droughts relative to ‘normal’ periods with high water table. We carried out controlled incubation experiments at 10°C on 10x10 cm peat soil cores collected from six UK sites across a sulphur deposition gradient. Our aim was to quantify the balance between microbial consumption and chemical precipitation of DOC due to episodic acidification driven by sulphur redox reactions by comparing changes in soil water chemistry to microbial activity (i.e. soil respiration and trace gas fluxes). During dry periods, all sites showed a concurrent increase in SO4 and soil respiration and a decline in DOC. However, the magnitude of change in both DOC and SO4 varied considerably between sites according to historical sulphur deposition loads and the variation in acid/base chemistry.

Processes controlling DOC in pore water during simulated drought cycles in six different UK peats

The effect of episodic drought on dissolved organic carbon (DOC) dynamics in peatlands has been the subject of considerable debate, as decomposition and DOC production is thought to increase under aerobic conditions, yet decreased DOC concentrations have been observed during drought periods. Decreased DOC solubility due to drought-induced acidification driven by sulphur (S) redox reactions has been proposed as a causal mechanism; however evidence is based on a limited number of studies carried out at a few sites. To test this hypothesis on a range of different peats, we carried out controlled drought simulation experiments on peat cores collected from six sites across Great Britain. Our data show a concurrent increase in sulphate (SO4) and a decrease in DOC across all sites during simulated water table draw-down, although the magnitude of the relationship between SO4 and DOC differed between sites. Instead, we found a consistent relationship across all sites between DOC decrease and acidification measured by the pore water acid neutralising capacity (ANC). ANC provided a more consistent measure of drought-induced acidification than SO4 alone because it accounts for differences in base cation and acid anions concentrations between sites. Rewetting resulted in rapid DOC increases without a concurrent increase in soil respiration, suggesting DOC changes were primarily controlled by soil acidity not soil biota. These results highlight the need for an integrated analysis of hydrologically driven chemical and biological processes in peatlands to improve our understanding and ability to predict the interaction between atmospheric pollution and changing climatic conditions from plot to regional and global scales.

Synthesis, structure, and redox states of homoleptic d-block metal complexes with bis-1,2,4-triazin-3-yl-pyridine and 1,2,4-triazin-3-yl-bipyridine extractants

it has been established that triazinyl bipyridines (hemi-BTPs) and bis-triazinyl pyridines (BTPs), ligands which are currently being investigated as possible ligands for the separation of actinides from lanthanides in nuclear waste, are able to form homoleptic complexes with first row transition metals such as cobalt(IT), copper(II), iron(II), manganese(II), nickel(II) and zinc(II). The metal complexes exhibit six-co-ordinate octahedral structures and redox states largely analogous to those of the related terpyridine complexes. The reactivity of the different redox states of cobalt bis-hemi-BTP complex in aqueous environments has been studied with two-phase electrochemistry by immobilisation of the essentially water-insoluble metal complexes on graphite electrodes and the immersion of this modified electrode in an aqueous electrolyte. It was found that redox potentials for the metal-centred reactions were pH-independent whereas the potentials for the ligand-centred reactions were strongly pH-dependent. The reductive degradation of these complexes has been investigated by computational methods. Solvent extraction experiments have been carried out for a range of metals and these show that cobalt(II) and nickel(II) as well as palladium(II), cadmium(II) and lead(II) were all extracted with the ligands 1e and 2c with higher distribution ratios that was observed for americium(III) under the same conditions. The implications of this result for the use of these ligands to separate actinides from nuclear waste are discussed. (c) 2005 Elsevier Ltd. All rights reserved.

Homogeneous and heterogeneous reactions of atmospheric mercury(II) with sulfur(IV)

Atmospheric models suggest that the reduction of Hg(II) to Hg(O) by S(W) prolongs the residence time of mercury. The redox reaction was investigated both in the aqueous phase (where the reductant is sulfite) and on particulate matter (where the reductant in SO2(g)). In both cases, one of the ultimate products is HgS. A mechanism is proposed involving formation of Hg(O) followed by mercury-induced disproportionation of SO2.

Syntheses, structures, some reactions, and electrochemical oxidation of ferrocenylethynyl complexes of iron, ruthenium, and osmium

The syntheses and characterizations of several complexes containing ferrocenylethynyl and ferrocene-1,1'-bis(ethynyl) groups attached to M(PP)Cp'[M = Fe, Ru, PP = dppe, Cp'= Cp*; M = Ru, Os, PP = (PPh3)(2), dppe, Cp' = Cp] are described. Reactions with tetracyanoethene have given either tetracyanobuta-1,3-dienyl or eta(3)-allylic derivatives, while addition of Me+ afforded the corresponding vinylidene derivatives. Some electrochemical measurements are discussed in terms of electronic communication between the redox-active M(PP)Cp' groups through the ferrocene nucleus. The molecular structures of 14 of these complexes have been determined by crystallographic methods.